Indole-3-carbinol-induced modulation of NF-κB signalling is breast cancer cell-specific and does not correlate with cell death

Breast Cancer Research and Treatment

Volumn 109, Issue 3, 2008, Pages 451-462

  Moiseeva, Elena P ^a   Heukers, Raimond ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Apoptosis; Breast cancer; Indole 3 carbinol; NF B

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 3 INDOLEMETHANOL; 4 (3 BROMOANILINO) 6,7 DIMETHOXYQUINAZOLINE; ACETYLSALICYLIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; I KAPPA B ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; ONCOPROTEIN; PROTEIN BCL XL; PROTEIN P68; PROTEIN SRC; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR REL; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BREAST CANCER; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DNA BINDING; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; SIGNAL TRANSDUCTION;

ANTICARCINOGENIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; CHROMONES; DNA; FEMALE; HUMANS; INDOLES; MORPHOLINES; NF-KAPPA B; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 43749118457     PISSN: 01676806     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10549-007-9669-6     Document Type: Article

References (76)

1. Parkin DM, Bray F, Ferlay J et al (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74-108
2. Gandini S, Merzenich H, Robertson C et al (2000) Meta-analysis of studies on breast cancer risk and diet: the role of fruit and vegetable consumption and the intake of associated micronutrients. Eur J Cancer 36:636-646
3. Dos Santos Silva I, Mangtani P, McCormack V et al (2002) Lifelong vegetarianism and risk of breast cancer: a population-based case-control study among South Asian migrant women living in England. Int J Cancer 99:238-244
4. Hermann S, Linseisen J, Chang-Claude J (2002) Nutrition and breast cancer risk by age 50: a population-based case-control study in Germany. Nutr Cancer 44:23-34
5. Hirose K, Takezaki T, Hamajima N et al (2003) Dietary factors protective against breast cancer in Japanese premenopausal and postmenopausal women. Int J Cancer 107:276-282
6. Sieri S, Krogh V, Pala V et al (2004) Dietary patterns and risk of breast cancer in the ORDET cohort. Cancer Epidemiol Biomarkers Prev 13:567-572
7. Fung TT, Hu FB, Holmes MD et al (2005) Dietary patterns and the risk of postmenopausal breast cancer. Int J Cancer 116:116-121
8. Ambrosone CB, McCann SE, Freudenheim JL et al (2004) Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. J Nutr 134:1134-1138
9. Pathak DR, He JP, Charzewska J (2005) Joint association of high cabbage/sauerkraut intake at 12-13 years of age and adulthood with reduced breast cancer risk in Polish migrant women: results from the US component of the Polish Womens Health Study (PWHS). Cancer Epidemiol Biomarkers Prev 14:2755S-2755S
10. Malloy VL, Bradlow HL, Orentreich N (1997) Interaction between a semisynthetic diet and indole-3-carbinol on mammary tumor incidence in Balb/cfC3H mice. Anticancer Res 17:4333-4337
11. Bradlow HL, Michnovicz J, Telang NT et al (1991) Effects of dietary indole-3-carbinol on estradiol metabolism and spontaneous mammary tumors in mice. Carcinogenesis 12:1571-1574
12. Rahman KM, Sarkar FH, Banerjee S et al (2006) Therapeutic intervention of experimental breast cancer bone metastasis by indole-3-carbinol in SCID-human mouse model. Mol Cancer Ther 5:2747-2756
13. Wattenberg LW, Loub WD (1978) Inhibition of polycyclic aromatic hydrocarbon-induced neoplasia by naturally occurring indoles. Cancer Res 38:1410-1413
14. Kojima T, Tanaka T, Mori H (1994) Chemoprevention of spontaneous endometrial cancer in female Donryu rats by dietary indole-3-carbinol. Cancer Res 54:1446-1449
15. Grubbs CJ, Steele VE, Casebolt T et al (1995) Chemoprevention of chemically-induced mammary carcinogenesis by indole-3-carbinol. Anticancer Res 15:709-716
16. Bell MC, Crowley-Nowick P, Bradlow HL et al (2000) Placebo-controlled trial of indole-3-carbinol in the treatment of CIN. Gynecol Oncol 78:123-129
17. Naik R, Nixon S, Lopes A et al (2006) A randomized phase II trial of indole-3-carbinol in the treatment of vulvar intraepithelial neoplasia. Int J Gynecol Cancer 16:786-790
18. Rosen CA, Bryson PC (2004) Indole-3-carbinol for recurrent respiratory papillomatosis: long-term results. J Voice 18:248-253
19. Malejka-Giganti D, Parkin DR, Bennett KK et al (2007) Suppression of mammary gland carcinogenesis by post-initiation treatment of rats with tamoxifen or indole-3-carbinol or their combination. Eur J Cancer Prev 16:130-141
20. Donald S, Verschoyle RD, Greaves P et al (2004) Dietary agent indole-3-carbinol protects female rats against the hepatotoxicity of the antitumor drug ET-743 (trabectidin) without compromising efficacy in a rat mammary carcinoma. Int J Cancer 111:961-967
21. Anderton MJ, Manson MM, Verschoyle RD et al (2004) Pharmacokinetics and tissue disposition of indole-3-carbinol and its acid condensation products after oral administration to mice. Clin Cancer Res 10:5233-5241
22. Reed GA, Arneson DW, Putnam WC et al (2006) Single-dose and multiple-dose administration of indole-3-carbinol to women: pharmacokinetics based on 3,3'-diindolylmethane. Cancer Epidemiol Biomarkers Prev 15:2477-2481
23. Crowell JA, Page JG, Levine BS et al (2006) Indole-3-carbinol, but not its major digestive product 3,3'-diindolylmethane, induces reversible hepatocyte hypertrophy and cytochromes P450. Toxicol Appl Pharmacol 211:115-123
24. Zhang X, Malejka-Giganti D (2003) Effects of treatment of rats with indole-3-carbinol on apoptosis in the mammary gland and mammary adenocarcinomas. Anticancer Res 23:2473-2479
25. Parkin DR, Malejka-Giganti D (2004) Differences in the hepatic P450-dependent metabolism of estrogen and tamoxifen in response to treatment of rats with 3,3'-diindolylmethane and its parent compound indole-3-carbinol. Cancer Detect Prev 28:72-79
26. Leibelt DA, Hedstrom OR, Fischer KA et al (2003) Evaluation of chronic dietary exposure to indole-3-carbinol and absorption-enhanced 3,3'-diindolylmethane in sprague-dawley rats. Toxicol Sci 74:10-21
27. Chinni SR, Sarkar FH (2002) Akt inactivation is a key event in indole-3-carbinol-induced apoptosis in PC-3 cells. Clin Cancer Res 8:1228-1236
28. Howells LM, Gallacher-Horley B, Houghton CE et al (2002) Indole-3-carbinol inhibits protein kinase B/Akt and induces apoptosis in the human breast tumor cell line MDA MB468 but not in the nontumorigenic HBL100 line. Mol Cancer Ther 1:1161-1172
29. Howells LM, Hudson EA, Manson MM (2005) Inhibition of phosphatidylinositol 3-kinase/protein kinase B signaling is not sufficient to account for indole-3-carbinol-induced apoptosis in some breast and prostate tumor cells. Clin Cancer Res 11:8521-8527
30. Moiseeva EP, Fox LH, Howells LM et al (2006) Indole-3-carbinol-induced death in cancer cells involves EGFR downregulation and is exacerbated in a 3D environment. Apoptosis 11:799-812
31. Moiseeva EP, Heukers R, Manson MM (2007) EGFR and Src are involved in indole-3-carbinol-induced death and cell cycle arrest of human breast cancer cells. Carcinogenesis 28:435-445
32. Chinni SR, Li Y, Upadhyay S et al (2001) Indole-3-carbinol (I3C) induced cell growth inhibition, G1 cell cycle arrest and apoptosis in prostate cancer cells. Oncogene 20:2927-2936
33. Takada Y, Andreeff M, Aggarwal BB (2005) Indole-3-carbinol suppresses NF-{kappa}B and I{kappa}B{alpha} kinase activation causing inhibition of expression of NF-{kappa}B-regulated antiapoptotic and metastatic gene products and enhancement of apoptosis in myeloid and leukemia cells. Blood 106:641-649
34. Kucharczak J, Simmons MJ, Fan Y et al (2003) To be, or not to be: NF-kappaB is the answer-role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene 22:8961-8982
35. Hoffmann A, Natoli G, Ghosh G (2006) Transcriptional regulation via the NF-kappaB signaling module. Oncogene 25:6706-6716
36. Karin M, Cao Y, Greten FR et al (2002) NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2:301-310
37. Rayet B, Gelinas C (1999) Aberrant rel/nfkb genes and activity in human cancer. Oncogene 18:6938-6947
38. Romieu-Mourez R, Kim DW, Shin SM et al (2003) Mouse mammary tumor virus c-rel transgenic mice develop mammary tumors. Mol Cell Biol 23:5738-5754
39. Varela LM, Stangle-Castor NC, Shoemaker SF et al (2001) TNFalpha induces NFkappaB/p50 in association with the growth and morphogenesis of normal and transformed rat mammary epithelial cells. J Cell Physiol 188:120-131
40. Landesman-Bollag E, Song DH, Romieu-Mourez R et al (2001) Protein kinase CK2: signaling and tumorigenesis in the mammary gland. Mol Cell Biochem 227:153-165
41. Bhat-Nakshatri P, Newton TR, Goulet R Jr et al (1998) NF-kappaB activation and interleukin 6 production in fibroblasts by estrogen receptor-negative breast cancer cell-derived interleukin 1alpha. Proc Natl Acad Sci USA 95:6971-6976
42. Pederson L, Winding B, Foged NT et al (1999) Identification of breast cancer cell line-derived paracrine factors that stimulate osteoclast activity. Cancer Res 59:5849-5855
43. Bhat-Nakshatri P, Sweeney CJ, Nakshatri H (2002) Identification of signal transduction pathways involved in constitutive NF-kappaB activation in breast cancer cells. Oncogene 21:2066-2078
44. Biswas DK, Cruz AP, Gansberger E et al (2000) Epidermal growth factor-induced nuclear factor kappa B activation: A major pathway of cell-cycle progression in estrogen-receptor negative breast cancer cells. Proc Natl Acad Sci USA 97:8542-8547
45. Madrid LV, Wang CY, Guttridge DC et al (2000) Akt suppresses apoptosis by stimulating the transactivation potential of the RelA/p65 subunit of NF-kappaB. Mol Cell Biol 20:1626-1638
46. Ali S, Kaur J, Patel KD (2000) Intercellular cell adhesion molecule-1, vascular cell adhesion molecule-1, and regulated on activation normal T cell expressed and secreted are expressed by human breast carcinoma cells and support eosinophil adhesion and activation. Am J Pathol 157:313-321
47. Newton TR, Patel NM, Bhat-Nakshatri P et al (1999) Negative regulation of transactivation function but not DNA binding of NF-kappaB and AP-1 by IkappaBbeta1 in breast cancer cells. J Biol Chem 274:18827-18835
48. Mendez O, Martin B, Sanz R et al (2006) Underexpression of transcriptional regulators is common in metastatic breast cancer cells overexpressing Bcl-xL. Carcinogenesis 27:1169-1179
49. Espana L, Fernandez Y, Rubio N et al (2004) Overexpression of Bcl-xL in human breast cancer cells enhances organ-selective lymph node metastasis. Breast Cancer Res Treat 87:33-44
50. Neve RM, Chin K, Fridlyand J et al (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10:515-527
51. Rice NR, MacKichan ML, Israel A (1992) The precursor of NF-kappa B p50 has I kappa B-like functions. Cell 71:243-253
52. Patel NM, Nozaki S, Shortle NH et al (2000) Paclitaxel sensitivity of breast cancer cells with constitutively active NF-kappaB is enhanced by IkappaBalpha super-repressor and parthenolide. Oncogene 19:4159-4169
53. Chen LF, Greene WC (2004) Shaping the nuclear action of NF-kappaB. Nat Rev Mol Cell Biol 5:392-401
54. Glasgow JN, Qiu J, Rassin D et al (2001) Transcriptional regulation of the BCL-X gene by NF-kappaB is an element of hypoxic responses in the rat brain. Neurochem Res 26:647-659
55. Gordon LA, Mulligan KT, Maxwell-Jones H et al (2003) Breast cell invasive potential relates to the myoepithelial phenotype. Int J Cancer 106:8-16
56. Yin MJ, Yamamoto Y, Gaynor RB (1998) The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature 396:77-80
57. Das R, Mahabeleshwar GH, Kundu GC (2003) Osteopontin stimulates cell motility and nuclear factor kappaB-mediated secretion of urokinase type plasminogen activator through phosphatidylinositol 3-kinase/Akt signaling pathways in breast cancer cells. J Biol Chem 278:28593-28606
58. Sliva D, Rizzo MT, English D (2002) Phosphatidylinositol 3-kinase and NF-kappaB regulate motility of invasive MDA-MB-231 human breast cancer cells by the secretion of urokinase-type plasminogen activator. J Biol Chem 277:3150-3157
59. Huang WC, Chen JJ, Chen CC (2003) c-Src-dependent tyrosine phosphorylation of IKKbeta is involved in tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 expression. J Biol Chem 278:9944-9952
60. Huang WC, Chen JJ, Inoue H et al (2003) Tyrosine phosphorylation of I-kappa B kinase alpha/beta by protein kinase C-dependent c-Src activation is involved in TNF-alpha-induced cyclooxygenase-2 expression. J Immunol 170:4767-4775
61. Jalal DI, Kone BC (2006) Src activation of NF-kappaB augments IL-1beta-induced nitric oxide production in mesangial cells. J Am Soc Nephrol 17:99-106
62. Qing G, Qu Z, Xiao G (2005) Regulation of NF-kappa B2 p100 processing by its cis-acting domain. J Biol Chem 280:18-27
63. Saccani S, Pantano S, Natoli G (2003) Modulation of NF-kappaB activity by exchange of dimers. Mol Cell 11:1563-1574
64. Moorthy AK, Ghosh G (2003) p105.Ikappa Bgamma and prototypical Ikappa Bs use a similar mechanism to bind but a different mechanism to regulate the subcellular localization of NF-kappa B. J Biol Chem 278:556-566
65. Lombaerts M, van Wezel T, Philippo K et al (2006) E-cadherin transcriptional downregulation by promoter methylation but not mutation is related to epithelial-to-mesenchymal transition in breast cancer cell lines. Br J Cancer 94:661-671
66. Funakoshi-Tago M, Tago K, Andoh K et al (2005) Functional role of c-Src in IL-1-induced NF-kappa B activation: c-Src is a component of the IKK complex. J Biochem (Tokyo) 137:189-197
67. Abu-Amer Y, Ross FP, McHugh KP et al (1998) Tumor necrosis factor-alpha activation of nuclear transcription factor-kappaB in marrow macrophages is mediated by c-Src tyrosine phosphorylation of Ikappa Balpha. J Biol Chem 273:29417-29423
68. Fan C, Li Q, Zhang Y et al (2004) IkappaBalpha and IkappaBbeta possess injury context-specific functions that uniquely influence hepatic NF-kappaB induction and inflammation. J Clin Invest 113:746-755
69. Habib AA, Chatterjee S, Park SK et al (2001) The epidermal growth factor receptor engages receptor interacting protein and nuclear factor-kappa B (NF-kappa B)-inducing kinase to activate NF-kappa B. Identification of a novel receptor-tyrosine kinase signalosome. J Biol Chem 276:8865-8874
70. Kapoor GS, Zhan Y, Johnson GR et al (2004) Distinct domains in the SHP-2 phosphatase differentially regulate epidermal growth factor receptor/NF-kappaB activation through Gab1 in glioblastoma cells. Mol Cell Biol 24:823-836
71. Beraud C, Henzel WJ, Baeuerle PA (1999) Involvement of regulatory and catalytic subunits of phosphoinositide 3-kinase in NF-kappaB activation. Proc Natl Acad Sci USA 96:429-434
72. Davies SP, Reddy H, Caivano M et al (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351:95-105
73. Monks NR, Pardee AB (2006) Targeting the NF-kappaB pathway in estrogen receptor negative MDA-MB-231 breast cancer cells using small inhibitory RNAs. J Cell Biochem 98:221-233
74. Chang HY, Yang X (2000) Proteases for cell suicide: functions and regulation of caspases. Microbiol Mol Biol Rev 64:821-846
75. Rahman KM, Li Y, Sarkar FH (2004) Inactivation of akt and NF-kappaB play important roles during indole-3-carbinol-induced apoptosis in breast cancer cells. Nutr Cancer 48:84-94
76. Kloth MT, Laughlin KK, Biscardi JS et al (2003) STAT5b, a mediator of synergism between c-Src and the epidermal growth factor receptor. J Biol Chem 278:1671-1679